Live-Cell Visualization of Pre-mRNA Splicing with Single-Molecule Sensitivity

Cell Reports

Volumn 4, Issue 6, 2013, Pages 1144-1155

  Martin, Robert M ^a   Rino, José ^a   Carvalho, Célia ^a   Kirchhausen, Tomas ^b   Carmo Fonseca, Maria ^a  

^a INSTITUTO DE MEDICINA MOLECULAR   (Portugal)

^b BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEMOGLOBIN BETA CHAIN; MESSENGER RNA PRECURSOR; RNA POLYMERASE II;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; EXON; GENETIC REGULATION; HUMAN; HUMAN CELL; INTRON; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN CLEAVAGE; PROTEIN LOCALIZATION; PROTEIN PROCESSING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA SPLICING; SPLICEOSOME; TRANSCRIPTION INITIATION SITE;

ANIMALS; BETA-GLOBINS; HELA CELLS; HUMANS; INTRONS; MICE; RNA SPLICE SITES; RNA SPLICING; RNA, MESSENGER;

EID: 84884595844     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2013.08.013     Document Type: Article

References (42)

1. Beyer A.L., Osheim Y.N. Splice site selection, rate of splicing, and alternative splicing on nascent transcripts. Genes Dev. 1988, 2:754-765.
2. Bhatt D.M., Pandya-Jones A., Tong A.J., Barozzi I., Lissner M.M., Natoli G., Black D.L., Smale S.T. Transcript dynamics of proinflammatory genes revealed by sequence analysis of subcellular RNA fractions. Cell 2012, 150:279-290.
3. Boulant S., Kural C., Zeeh J.C., Ubelmann F., Kirchhausen T. Actin dynamics counteract membrane tension during clathrin-mediated endocytosis. Nat. Cell Biol. 2011, 13:1124-1131.
4. Chubb J.R., Liverpool T.B. Bursts and pulses: insights from singlecell studies into transcriptional mechanisms. Curr. Opin. Genet. Dev. 2010, 20:478-484.
5. Cooper T.A., Wan L., Dreyfuss G. RNA and disease. Cell 2009, 136:777-793.
6. Corrionero A., Miñana B., Valcárcel J. Reduced fidelity of branchpoint recognition and alternative splicing induced by the anti-tumor drug spliceostatin A. Genes Dev. 2011, 25:445-459.
7. Custódio N., Carmo-Fonseca M., Geraghty F., Pereira H.S., Grosveld F., Antoniou M. Inefficient processing impairs release of RNA from the site of transcription. EMBO J. 1999, 18:2855-2866.
8. Daigle N., Ellenberg J. LambdaN-GFP: an RNA reporter system for live-cell imaging. Nat. Methods 2007, 4:633-636.
9. Danko C.G., Hah N., Luo X., Martins A.L., Core L., Lis J.T., Siepel A., Kraus W.L. Signaling pathways differentially affect RNA polymerase II initiation, pausing, and elongation rate in cells. Mol. Cell 2013, 50:212-222.
10. Darzacq X., Shav-Tal Y., de Turris V., Brody Y., Shenoy S.M., Phair R.D., Singer R.H. Invivo dynamics of RNA polymerase II transcription. Nat. Struct. Mol. Biol. 2007, 14:796-806.
11. Das R., Dufu K., Romney B., Feldt M., Elenko M., Reed R. Functional coupling of RNAP II transcription to spliceosome assembly. Genes Dev. 2006, 20:1100-1109.
12. de Almeida S.F., García-Sacristán A., Custódio N., Carmo-Fonseca M. A link between nuclear RNA surveillance, the human exosome and RNA polymerase II transcriptional termination. Nucleic Acids Res. 2010, 38:8015-8026.
13. de la Mata M., Alonso C.R., Kadener S., Fededa J.P., Blaustein M., Pelisch F., Cramer P., Bentley D., Kornblihtt A.R. A slow RNA polymerase II affects alternative splicing invivo. Mol. Cell 2003, 12:525-532.
14. Dye M.J., Proudfoot N.J. Terminal exon definition occurs cotranscriptionally and promotes termination of RNA polymerase II. Mol. Cell 1999, 3:371-378.
15. Eperon L.P., Graham I.R., Griffiths A.D., Eperon I.C. Effects of RNA secondary structure on alternative splicing of pre-mRNA: is folding limited to a region behind the transcribing RNA polymerase?. Cell 1988, 54:393-401.
16. Franklin N.C. Conservation of genome form but not sequence in the transcription antitermination determinants of bacteriophages lambda, phi 21 and P22. J.Mol. Biol. 1985, 181:75-84.
17. Grünwald D., Singer R.H. Invivo imaging of labelled endogenous β-actin mRNA during nucleocytoplasmic transport. Nature 2010, 467:604-607.
18. Hocine S., Raymond P., Zenklusen D., Chao J.A., Singer R.H. Single-molecule analysis of gene expression using two-color RNA labeling in live yeast. Nat. Methods 2013, 10:119-121.
19. Hoskins A.A., Friedman L.J., Gallagher S.S., Crawford D.J., Anderson E.G., Wombacher R., Ramirez N., Cornish V.W., Gelles J., Moore M.J. Ordered and dynamic assembly of single spliceosomes. Science 2011, 331:1289-1295.
20. Kaida D., Motoyoshi H., Tashiro E., Nojima T., Hagiwara M., Ishigami K., Watanabe H., Kitahara T., Yoshida T., Nakajima H., et al. Spliceostatin A targets SF3b and inhibits both splicing and nuclear retention of pre-mRNA. Nat. Chem. Biol. 2007, 3:576-583.
21. Kessler O., Jiang Y., Chasin L.A. Order of intron removal during splicing of endogenous adenine phosphoribosyltransferase and dihydrofolate reductase pre-mRNA. Mol. Cell. Biol. 1993, 13:6211-6222.
22. Kural C., Tacheva-Grigorova S.K., Boulant S., Cocucci E., Baust T., Duarte D., Kirchhausen T. Dynamics of intracellular clathrin/AP1- and clathrin/AP3-containing carriers. Cell Rep. 2012, 2:1111-1119.
23. Larson D.R., Zenklusen D., Wu B., Chao J.A., Singer R.H. Real-time observation of transcription initiation and elongation on an endogenous yeast gene. Science 2011, 332:475-478.
24. Lionnet T., Czaplinski K., Darzacq X., Shav-Tal Y., Wells A.L., Chao J.A., Park H.Y., de Turris V., Lopez-Jones M., Singer R.H. A transgenic mouse for invivo detection of endogenous labeled mRNA. Nat. Methods 2011, 8:165-170.
25. Lowary P.T., Uhlenbeck O.C. An RNA mutation that increases the affinity of an RNA-protein interaction. Nucleic Acids Res. 1987, 15:10483-10493.
26. Maniatis T., Reed R. An extensive network of coupling among gene expression machines. Nature 2002, 416:499-506.
27. Martins S.B., Rino J., Carvalho T., Carvalho C., Yoshida M., Klose J.M., de Almeida S.F., Carmo-Fonseca M. Spliceosome assembly is coupled to RNA polymerase II dynamics at the 3' end of human genes. Nat. Struct. Mol. Biol. 2011, 18:1115-1123.
28. Nilsen T.W., Graveley B.R. Expansion of the eukaryotic proteome by alternative splicing. Nature 2010, 463:457-463.
29. Niwa M., MacDonald C.C., Berget S.M. Are vertebrate exons scanned during splice-site selection?. Nature 1992, 360:277-280.
30. Nogues G., Kadener S., Cramer P., Bentley D., Kornblihtt A.R. Transcriptional activators differ in their abilities to control alternative splicing. J.Biol. Chem. 2002, 277:43110-43114.
31. Roybal G.A., Jurica M.S. Spliceostatin A inhibits spliceosome assembly subsequent to prespliceosome formation. Nucleic Acids Res. 2010, 38:6664-6672.
32. Shav-Tal Y., Darzacq X., Shenoy S.M., Fusco D., Janicki S.M., Spector D.L., Singer R.H. Dynamics of single mRNPs in nuclei of living cells. Science 2004, 304:1797-1800.
33. Singh J., Padgett R.A. Rates of insitu transcription and splicing in large human genes. Nat. Struct. Mol. Biol. 2009, 16:1128-1133.
34. Staley J.P., Guthrie C. Mechanical devices of the spliceosome: motors, clocks, springs, and things. Cell 1998, 92:315-326.
35. Tsurushita N., Avdalovic N.M., Korn L.J. Regulation of differential processing of mouse immunoglobulin mu heavy-chain mRNA. Nucleic Acids Res. 1987, 15:4603-4615.
36. Valegård K., Murray J.B., Stockley P.G., Stonehouse N.J., Liljas L. Crystal structure of an RNA bacteriophage coat protein-operator complex. Nature 1994, 371:623-626.
37. Vargas D.Y., Shah K., Batish M., Levandoski M., Sinha S., Marras S.A., Schedl P., Tyagi S. Single-molecule imaging of transcriptionally coupled and uncoupled splicing. Cell 2011, 147:1054-1065.
38. Watakabe A., Inoue K., Sakamoto H., Shimura Y. A secondary structure at the 3' splice site affects the invitro splicing reaction of mouse immunoglobulin mu chain pre-mRNAs. Nucleic Acids Res. 1989, 17:8159-8169.
39. Watakabe A., Tanaka K., Shimura Y. The role of exon sequences in splice site selection. Genes Dev. 1993, 7:407-418.
40. Wetterberg I., Zhao J., Masich S., Wieslander L., Skoglund U. Insitu transcription and splicing in the Balbiani ring 3 gene. EMBO J. 2001, 20:2564-2574.
41. Will C.L., Lührmann R. Spliceosome structure and function. ColdSpring Harb. Perspect. Biol. 2011, 3:3.
42. Wu B., Chao J.A., Singer R.H. Fluorescence fluctuation spectroscopy enables quantitative imaging of single mRNAs in living cells. Biophys. J. 2012, 102:2936-2944.